Receptive fields and dendritic structure of directionally selective retinal ganglion cells

We studied the relationship between the receptive fields of directionally selective retinal ganglion cells and the dendritic arbors of the same cells. The cells were recorded from extracellularly under visual control and then injected with Lucifer yellow. The arbor of Lucifer-filled dendrites could then be directly compared with the properties of the receptive field. A large population of on-off directionally selective cells was injected and drawn. The directionally selective ganglion cells had bistratified receptive fields similar to those previously described by others in the central retina. In the periphery, the dendritic fields became larger, rounder, and sparser than centrally. The diameters of the dendrites were measured in living or lightly fixed retinas; they were found to be somewhat larger than previously estimated by electron microscopy. The local structure of the dendritic arbor bore no obvious relation to the directional properties of the cell. The receptive fields of most cells were centered symmetrically around their dendritic fields. For about 10% of the cells, however, the receptive field was displaced. The displacement was always toward the preferred direction, relative to the dendritic field. The meaning of these shifts is not clear. In both cases, the diameter of the receptive field exceeded the diameter of the dendritic field only slightly; in our sample, the diameters of the receptive fields averaged 6% larger than the dendritic fields. This means that the neurons afferent to the directionally selective ganglion cells must either have narrow dendritic fields or, if they are wide spreading, have dendrites that do not conduct effectively along their length. It also means that the observed spread of neurobiotin between DS ganglion cells (Vaney, 1991) must be due to a very few gap junctions, or to some mechanism other than a gap junction.

[1]  H. Barlow,et al.  The mechanism of directionally selective units in rabbit's retina. , 1965, The Journal of physiology.

[2]  R. Dacheux,et al.  Horizontal cells in the retina of the rabbit , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  S. Bloomfield,et al.  Relationship between receptive and dendritic field size of amacrine cells in the rabbit retina. , 1992, Journal of neurophysiology.

[4]  C. W. Oyster,et al.  The analysis of image motion by the rabbit retina , 1968, The Journal of physiology.

[5]  S. Bloomfield Two types of orientation-sensitive responses of amacrine cells in the mammalian retina , 1991, Nature.

[6]  N. Grzywacz,et al.  A model of the directional selectivity circuit in retina: transformations by neurons singly and in concert , 1992 .

[7]  F. Amthor,et al.  Morphology of on-off direction-selective ganglion cells in the rabbit retina , 1984, Brain Research.

[8]  S. Bloomfield,et al.  Electroanatomy of a unique amacrine cell in the rabbit retina. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[9]  R H Masland,et al.  Responses to acetylcholine of ganglion cells in an isolated mammalian retina. , 1976, Journal of neurophysiology.

[10]  R. Masland,et al.  Local order among the dendrites of an amacrine cell population , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  A. Ames,et al.  In Vitro Retina as an Experimental Model of the Central Nervous System , 1981, Journal of neurochemistry.

[12]  Christopher Brandon,et al.  Cholinergic neurons in the rabbit retina: dendritic branching and ultrastructural connectivity , 1987, Brain Research.

[13]  E. V. Famiglietti,et al.  Dendritic Co‐stratification of ON and ON‐OFF directionally selective ganglion cells with starburst amacrine cells in rabbit retina , 1992, The Journal of comparative neurology.

[14]  R. Masland,et al.  The functions of acetylcholine in the rabbit retina , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[15]  D. I. Vaney,et al.  Chapter 2 The mosaic of amacrine cells in the mammalian retina , 1990 .

[16]  T. Poggio,et al.  A synaptic mechanism possibly underlying directional selectivity to motion , 1978, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[17]  H. Wässle,et al.  Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and gamma-aminobutyrate immunoreactivity. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Wilfrid Rall,et al.  Theoretical significance of dendritic trees for neuronal input-output relations , 1964 .

[19]  F. Amthor,et al.  Morphologies of rabbit retinal ganglion cells with complex receptive fields , 1989, The Journal of comparative neurology.

[20]  R. Yuste,et al.  Extensive dye coupling between rat neocortical neurons during the period of circuit formation , 1993, Neuron.

[21]  D. I. Vaney,et al.  ‘Coronate’ amacrine cells in the rabbit retina have the ‘starburst’ dendritic morphology , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[22]  D. I. Vaney,et al.  Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin , 1991, Neuroscience Letters.

[23]  R H Masland,et al.  The shape and arrangement of the cholinergic neurons in the rabbit retina , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[24]  H. Wässle,et al.  The structural correlate of the receptive field centre of alpha ganglion cells in the cat retina. , 1983, The Journal of physiology.

[25]  D. Mastronarde Interactions between ganglion cells in cat retina. , 1983, Journal of neurophysiology.

[26]  M. Ariel,et al.  Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells , 1982, The Journal of physiology.

[27]  E. V. Famiglietti,et al.  Synaptic organization of starburst amacrine cells in rabbit retina: Analysis of serial thin sections by electron microscopy and graphic reconstruction , 1991, The Journal of comparative neurology.

[28]  E. V. Famiglietti,et al.  ‘Starburst’ amacrine cells and cholinergic neurons: mirror-symmetric ON and OFF amacrine cells of rabbit retina , 1983, Brain Research.

[29]  N. Daw,et al.  Directionally sensitive ganglion cells in the rabbit retina: specificity for stimulus direction, size, and speed. , 1975, Journal of neurophysiology.

[30]  T. Poggio,et al.  Retinal ganglion cells: a functional interpretation of dendritic morphology. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[31]  R H Masland,et al.  Direct visualization of the dendritic and receptive fields of directionally selective retinal ganglion cells. , 1992, Science.